Figure-ground discrimination by relative movement in the visual system of the fly (original) (raw)

Neural circuit tuning fly visual neurons to motion of small objects. II. Input organization of inhibitory circuit elements revealed by electrophysiological and optical recording techniques

Journal of Neurophysiology

1. The FD1-cell in the visual system of the fly is an identified visual interneuron that is specifically tuned to motion of small objects. In the companion paper it was shown that this response property is mediated by one of the two CH-cells, the VCH-cell, that inhibits the FD1-cell by GABAergic synapses. Here the input organization of the two CH-cells is analyzed by both electrophysiological and optical recording techniques. 2. Both CH-cells are excited by front-to-back motion in the ipsilateral and by back-to-front motion in the contralateral visual field. They respond maximally to binocular rotatory motion about the vertical axis of the animal. The latter response is only slightly less than the sum of the corresponding monocular response components. The relative contribution of the ipsi-and contralateral eye to the binocular response varies considerably between flies. In extreme cases it is dominated by either the ipsi- or the contralateral eye. The two CH-cells are not equally s...

Neural circuit tuning fly visual neurons to motion of small objects. II. Input organization of inhibitory circuit elements revealed by electrophysiological and optical …

Journal of …, 1993

I. The FDl-cell in the visual system of the fly is an identified visual interneuron that is specifically tuned to motion of small objects. In the companion paper it was shown that this response property is mediated by one of the two CH-cells, the VCH-cell, that inhibits the FDl-cell by GABAergic synapses. Here the input organization of the two CH-cells is analyzed by both electrophysiological and optical recording techniques. 2. Both CH-cells arc excited by front-to-back motion in the ipsilateral and by back-to-front motion in the contralateral visual field. They respond maximally to binocular rotatory motion about the vertical axis of the animal. The latter response is only slightly less than the sum of the corresponding monocular response components. The relative contribution of the ipsi-and contralateral eye to the binocular response varies considerably between flies. In extreme cases it is dominated by either the ipsi-or the contralateral eye. The two CH-cells are not equally sensitive along the vertical axis of the eye. The DCH-cell has its sensitivity maximum in the dorsal part, the VCH-cell in the ventral part of the visual field. 3. The CH-cells have two arborizations, a large one in the posterior part of the third visual neuropil, the lobula plate, and a smaller one in the ipsilateral ventrolateral brain. With the calcium-sensitive dye fura-as an activity marker, it is analyzed which of these branches of the CH-cells receive the ipsi-and contralateral motion input, respectively. During motion in the preferred direction within the ipsilateral visual held, calcium accumulates only in the CH-cells' main arborization in the lobula plate but not in their branches in the ventrolateral brain, indicating that the arborization in the lobula plate is postsynaptic to the ipsilateral input. In contrast, contralateral motion in the preferred direction leads to calcium accumulation in both arborizations, suggesting that both are postsynaptic to contralateral input elements. During preferred direction motion in the upper or lower part of the ipsilateral visual field, calcium accumulates in only dorsal or ventral branches of the CH-cells' arborization in the lobula plate, respectively, revealing that their ipsilateral motion input is organized retinotopically. Because this arborization, most likely, is also the main output terminal of the CH-cells, it is both pre-and postsynaptic. This specific neuronal design is discussed with respect to its consequences for the mechanism of tuning the FD l-cell to motion of small objects.

Warzecha, A. K., Egelhaaf, M. & Borst, A. Neural circuit tuning fly visual interneurons to motion of small objects. I. Dissection of the circuit by pharmacological and photoinactivation techniques. J. Neurophysiol. 69, 329-339

Journal of Neurophysiology

1. Visual interneurons tuned to the motion of small objects are found in many animal species and are assumed to be the neuronal basis of figure-ground discrimination by relative motion. A well-examined example is the FD1-cell in the third visual neuropil of blowflies. This cell type responds best to motion of small objects. Motion of extended patterns elicits only small responses. As a neuronal mechanism that leads to such a response characteristic, it was proposed that the FD1-cell is inhibited by the two presumably GABAergic and, thus, inhibitory CH-cells, the VCH-and the DCH-cell. The CH-cells respond best to exactly that type of motion by which the activity of the FD1-cell is reduced. The hypothesis that the CH-cells inhibit the FD1-cell and, thus, mediate its selectivity to small moving objects was tested by ablating the CH-cells either pharmacologically or by photoinactivation. 2. After application of the [gamma]-aminobutyric acid (GABA) antagonist picrotoxinin, the FD1-cell responds more strongly to large-field than to small-field motion, i.e., it has lost its small-field selectivity. This suggests that the tuning of the FD1-cell to small moving objects relies on a GABAergic mechanism and, thus, most likely on the CH-cells. 3. The role of each CH-cell for small-field tuning was determined by inactivating them individually. They were injected with a fluorescent dye and then ablated by laser illumination. Only photoinactivation of the VCH-cell eliminated the specific selectivity of the FD1-cell for small-field motion. Ablation of the DCH-cell did not significantly change the response characteristic of the FD1-cell. This reveals the important role of the VCH-cells in mediating the characteristic sensitivity of the FD1-cell to motion of small objects. 4. The FD1-cell is most sensitive to motion of small objects in the ventral part of the ipsilateral visual field, whereas motion in the dorsal part influences the cell only weakly. This specific feature fits well to the sensitivity of the VCH-cell to ipsilateral motion that is most pronounced in the ventral part of the visual field. The spatial sensitivity distribution of the FD1-cell matches also the characteristics of figure-ground discrimination and fixation behavior. JOI JKNAL.

Neural circuit tuning fly visual interneurons to motion of small objects. I. Dissection of the circuit by pharmacological and photoinactivation techniques

Journal of Neurophysiology

1. Visual interneurons tuned to the motion of small objects are found in many animal species and are assumed to be the neuronal basis of figure-ground discrimination by relative motion. A well-examined example is the FD1-cell in the third visual neuropil of blowflies. This cell type responds best to motion of small objects. Motion of extended patterns elicits only small responses. As a neuronal mechanism that leads to such a response characteristic, it was proposed that the FD1-cell is inhibited by the two presumably GABAergic and, thus, inhibitory CH-cells, the VCH- and the DCH-cell. The CH-cells respond best to exactly that type of motion by which the activity of the FD1-cell is reduced. The hypothesis that the CH-cells inhibit the FD1-cell and, thus, mediate its selectivity to small moving objects was tested by ablating the CH-cells either pharmacologically or by photoinactivation. 2. After application of the gamma-aminobutyric acid (GABA) antagonist picrotoxinin, the FD1-cell re...

Directionally Selective Motion Detection by Insect Neurons

Facets of Vision (D.G. Stavenge and R.C. Hardie, eds.) Springer, Berlin, Germany, 1989

ABSTRACT Animals have several good reasons for detecting motion with their eyes. First, the motion of other animals — potential preys, mates, intruders or predators — provides essential information on which to base vital moves such as escape or chase. Secondly, information about self-motion is crucial, especially in the context of navigation, course stabilization, obstacle avoidance, and collision-free goal reaching. In fact, the wealth of information provided by passive, non-contact self-motion evaluation in visual systems has been likened to a kind of “visual kinaesthesis” (Gibson 1958). Even the 3D structure of the environment can be picked up by a moving observer (revs. Collett and Harkness 1982; Buchner 1984; Nakayama 1985; Hildreth and Koch 1987). Von Helmholtz (1867) was the first to clearly state the importance of this “motion parallax” in locomotion, and Exner (1891) proposed that arthropods make use of motion parallax as well as stereopsis to estimate distances (see also Horridge 1986)...

Computational structure of a biological motion-detection system as revealed by local detector analysis in the fly’s nervous system

Journal of the Optical Society of America A, 1989

The computations performed by individual movement detectors are analyzed by intracellularly recording from an identified direction-selective motion-sensitive interneuron in the fly's brain and by comparing these results with model predictions based on movement detectors of the correlation type. Three main conclusions were drawn with respect to the movement-detection system of the fly: (1) The essential nonlinear interaction between the two movement-detector input channels can be characterized formally by a mathematically almost perfect multiplication process. (2) Even at high contrasts no significant nonlinearities seem to distort the time course of the movement-detector input signals. (3) The movement detectors of the fly are not perfectly antisymmetrical; i.e., they respond with different time courses and amplitudes to motion in their preferred and null directions. As a consequence of this property, the motion detectors can respond to some degree to stationary patterns whose brightness is modulated in time. Moreover, the direction selectivity, i.e., the relative difference of the responses to motion in the preferred and null directions, depends on the contrast and on the spatial-frequency content of the stimulus pattern.